Abstract

Plastocyanin (PC) is an essential and abundant copper (Cu) protein required for photosynthesis in higher plants. Severe copper deprivation has the potential to cause a defect in photosynthetic electron transport due to a lack in PC. The Cu-microRNAs, which are up-regulated under Cu deficiency, down-regulate the expression of target Cu proteins other than PC, cytochrome-c oxidase and the ethylene receptors. It has been proposed that this mechanism saves Cu for PC maturation. We aimed to test how hybrid poplar, a species that has capacity to rapidly expand its photosynthetically active tissue, responds to variations in Cu availability over time. Measurement of chlorophyll fluorescence after Cu depletion revealed a drastic effect on photosynthesis in hybrid poplar. The decrease in photosynthetic capacity was correlated with a reduction in PC protein levels. Compared to older leaves, PC decreased more strongly in developing leaves, which also lost more photosynthetic electron transport capacity. The effect of Cu depletion on older and more developed leaves was minor and these leaves maintained much of their photosynthetic capacity. Interestingly, upon resupply of Cu to the medium a very rapid recovery of Cu levels was seen in the younger leaves with a concomitant rise in the expression and activity of PC. In contrast, the expression of those Cu proteins, which are targets of microRNAs was under the same circumstances delayed. At the same time, Cu resupply had only minor effects on the older leaves. The data suggest a model where rapid recovery of photosynthetic capacity in younger leaves is made possible by a preferred allocation of Cu to PC in younger leaves, which is supported by Cu-microRNA expression.

Highlights

  • Copper (Cu) is a redox-active transition metal essential for plant growth and development

  • Because we are especially interested in Cu homeostasis in the context of photosynthesis we aimed to analyze the response of the photosynthetic machinery to varying Cu supply in hybrid poplar

  • The 50 nM CuSO4 concentration in the control medium was previously shown to be sufficient for a range of plants (Cohu and Pilon, 2007) and allowed for vigorous growth of hybrid poplar (Figure 1A)

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Summary

Introduction

Copper (Cu) is a redox-active transition metal essential for plant growth and development. Cu-proteins in plants include PC, cytochrome-c oxidase, the ethylene receptors, copper/zinc superoxide dismutase (Cu/ZnSOD), ascorbate oxidase, amine-oxidase, laccase (LAC), plantacyanin and polyphenol oxidase (PPO; for a review see: Cohu and Pilon, 2010). Cu economy in hybrid poplar the most abundant plant Cu proteins are found in the chloroplasts: PC, Cu/ZnSOD, and PPO. PC is a single Cu atom containing protein located in the thylakoid lumen that is essential for photosynthetic electron transport in plants (Weigel et al, 2003). In Arabidopsis plantacyanin is thought to have a role in reproduction perhaps by mediating pollen tube growth (Dong et al, 2005). PPO is found in several plants including poplar (Constabel et al, 2000; Ravet et al, 2011), but missing in Arabidopsis thaliana (Schubert et al, 2002). PPO was proposed to function in defense against herbivory (Wang and Constabel, 2004)

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